A Mid-Cretaceous Ectoparasitic Fungus, Spheciophila adercia gen et sp. nov., Attached to a Wasp in Myanmar Amber

Abstract

A mid-Cretaceous ectoparasitic fungus in Myanmar amber is described as Spheciophila adercia gen. et sp. nov. in the new Family Spheciophilaceae fam. nov. While the specimen shares an ectoparasitic habit with representatives of the Laboulbeniales, morphological and behavioral features are not consistent with members of that group. The fossil is attached to the abdominal tergite of a primitive wasp. Its presence establishes a unique lineage of ectoparasitic insect fungi in the mid-Cretaceous. The present paper describes this interesting fossil, which adds to the diversity of ectoparasitic fungi and their insect hosts some 100 mya.

Full text

Volume 6 • Issue 2 • 1000145
Fungal Genom Biol, an open access journal
ISSN: 2165-8056
Research Article
Fungal Genomics & Biology
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ISSN: 2165-8056
Poinar Jr, Fungal Genom Biol 2016, 6:2
DOI: 10.4172/2165-8056.1000145
OMICS International
*Corresponding author: George Poinar Jr., Department of Integrative Biology,
Oregon State University, Corvallis, OR, 97331 USA, Tel: 5417607319; Fax:
5417571639; E-mail: poinarg@science.oregonstate.edu
Received October 24, 2016; Accepted November 21, 2016; Published November
29, 2016
Citation: Poinar Jr G (2016) A Mid-Cretaceous Ectoparasitic Fungus, Spheciophila
adercia gen et sp. nov., Attached to a Wasp in Myanmar Amber. Fungal Genom Biol
6: 145. doi:10.4172/2165-8056.1000145
Copyright: © 2016 Poinar Jr G. This is an open-access article distributed under
the terms of the Creative Commons Attribution License, which permits unrestricted
use, distribution, and reproduction in any medium, provided the original author and
source are credited.
A Mid-Cretaceous Ectoparasitic Fungus,
Spheciophila adercia
gen et sp.
nov., Attached to a Wasp in Myanmar Amber
George Poinar Jr.*
Department of Integrative Biology, Oregon State University, Corvallis, OR, 97331 USA
Abstract
A mid-Cretaceous ectoparasitic fungus in Myanmar amber is described as Spheciophila adercia gen. et sp. nov. in
the new Family Spheciophilaceae fam. nov. While the specimen shares an ectoparasitic habit with representatives of
the Laboulbeniales, morphological and behavioral features are not consistent with members of that group. The fossil
is attached to the abdominal tergite of a primitive wasp. Its presence establishes a unique lineage of ectoparasitic
insect fungi in the mid-Cretaceous. The present paper describes this interesting fossil, which adds to the diversity of
ectoparasitic fungi and their insect hosts some 100 mya.
Keywords: Ectoparasitic fungus; Myanmar amber; Spheciophila
adercia gen et sp. nov
Introduction
e fossil record of entomogenous fungi is not extensive, with most
cases representing ectoparasitic forms found on the body surface of
insects in Tertiary amber [1-3]. Today, while several groups of fungi
parasitize the integument of arthropods [4,5], the most common
and only group that forms thalli on the surface of arthropods is the
Laboulbeniales [6,7]. is Order consists of small, microscopic obligate
ectoparasites that normally occur on the integument of their hosts.
e Laboulbeniales produce thalli directly from ascospores that stick
to the integument of the host. In contrast to most fungi, mycelium is
not produced. e thalli, which contain a three-celled receptacle with a
single point of attachment to the host, can occur on many dierent sites
on the body of the host. Spermatia produced in antheridial appendages
fertilize perithecia, with the latter forming the major portion of the
thallus. Nourishment is obtained through the foot (haustorium) of
the fungus that is embedded in the host’s cuticle. In some cases, as in
members of the genus Hesperomyces, the haustoria extend through the
body wall and obtain nutrients from the haemocoel [8].
is cosmopolitan group of fungi parasitizes invertebrates in soil,
water and decomposing plant and animal matter, although the majority
of hosts are beetles (Coleoptera) [6-13]. While the present fossil has some
characteristics of members of the Laboulbeniales, other morphological
and behavioral features are not consistent with those of this group, which
is why it is described as a new genus and species in an extinct family. is
interesting and unusual fossil adds to the biodiversity of ectoparasitic
fungi and their hosts that existed some 100 mya.
Materials and Methods
e specimen originated from the Noije Bum 2001 Summit Site
mine excavated in the Hukawng Valley in 2001 and located southwest
of Maingkhwan in Kachin State (26º20´N, 96º36´E) in Myanmar. Based
on paleontological evidence this site was dated to the late Albian of the
Early Cretaceous [14], placing the age at 97 to 110 mya. A more recent
study using U-Pb zircon dating determined the age to be 98.79 ± 0.62
Ma or at the Albian/Cenomanian boundary [15]. Nuclear magnetic
resonance (NMR) spectra and the presence of araucaroid wood bers
in amber samples from the Noije Bum, 2001 Summit Site indicates an
araucarian tree source for the amber [16].
Observations and photographs were made with a Nikon SMZ-10 R
stereoscopic microscope and Nikon Optiphot compound microscope
with magnications up to 800 X. Terminology follows that used by
Benjamin [6] and Tavares [7] for Laboulbeniales.
Results
Detailed observations on the cellular structure of the perithecia
and antheridia were hindered by the thickness of the amber and a
viscous deposit surrounding the thallus (Figure 1). Also, since the
host’s integument is black, it was not possible to view the specimen in
transmitted light.
Description
Kingdom: Fungi
Division: Ascomycota
Class: “Incertae Sedis”
Order: “Incertae Sedis”
Spheciophilaceae fam. nov. (MycoBank # = 819144)
Type genus: Spheciophila Poinar gen. Nov.
Diagnosis: As for type species (monotypic)
Genus Spheciophila Poinar, gen. nov. (MycoBank # = 819145)
Type species: Spheciophila adercia Poinar gen. et sp. nov.
Spheciophila adercia Poinar gen. et sp. nov. (MycoBank # = 819146)
(Figures 1-4)
allus growing prostrate on host, opaque with thick cell walls, 1.05
mm in total length; consisting of a single stalk of ve erect cells with

Citation: Poinar Jr G (2016) A Mid-Cretaceous Ectoparasitic Fungus, Spheciophila adercia gen et sp. nov., Attached to a Wasp in Myanmar Amber.
Fungal Genom Biol 6: 145. doi:10.4172/2165-8056.1000145
Page 2 of 4
Volume 6 • Issue 2 • 1000145
Fungal Genom Biol
ISSN: 2165-8056 FGB, an open access journal
a terminal portion bent at an angle of 90 degrees bearing antheridia
and perithecia. Basal cell (I) short, suprabasal cell (II) slightly longer
and curved, cell III long, robust and triangular-shaped, cells IV and
V straight and subequal in length (Figure 2). Filamentous setaceous
conidial and sterile appendages occur sporadically on the surfaces of
the stalk cells. e terminal bent portion anterior to cell V contains
some 22 short compact cells bearing perithecia, antheridia and
sterile appendages. e perithecia are ask-shaped with terminal or
subterminal appendages that resemble trichogynes. Just prior to and
below the bent terminal portion of the primary stalk is a tued branch
that is attached at its base to the primary stalk. e tued branch bears
numerous antheridial receptacle cells with developing endogenous
spermatia. Measurements: Cell I: length, 70 µm; greatest width, 53 µm;
Cell II: length, 140 µm; greatest width, 55 µm; Cell III: length, 245 µm;
greatest width, 160 µm; length primary stalk, 580 µm; width primary
stalk 55 µm; length tued branch, 230 µm; width tued branch, 70
µm; length developing perithecia, 62 µm-64 µm; length extended tip
of perithecia, 12 µm-14 µm long; maturing antheridial receptacle cells
from 26 µm-45 µm in length.
Diagnosis
e multi-celled receptacle with a single point of attachment to the
host, spermatia produced in antheridial appendages and the presence
of perithecia are features of Spheciophila adercia gen et sp. nov. that also
occur in members of the Laboulbeniales [6,7]. However, the large size
of the thallus (in most species of Laboulbeniales, the thallus is under 1
Figure 1: Thallus of Spheciophila adercia gen. et sp. nov. (large arrow) attached
to the abdominal segment of its hymenopteran host in Myanmar amber.
Small arrow shows viscous droplet partly surrounding thallus. Bar=72 µm
Figure 3: Drawing of the thallus of Spheciophila adercia gen. et sp. nov. in
Myanmar amber with additional features and inserts of photos from different
regions of the fossil.
A=Vertical conidial branch; F=Flattened area on terminal receptacle cell where
a secondary stalk may have broken off; P=Region of perithecia on bent portion
of primary stalk. Arrowheads show two perithecia. S=Primary stalk that
bends approximately 90˚ degrees inwards and contains some 22 short
compact cells bearing perithecia, antheridia and sterile appendages. T=Bent
portion of stalk and antheridial-bearing tufted branch that is attached at its base
to the primary stalk. Bar=130 µm
Figure 2: Thallus of Spheciophila adercia gen. et sp. nov. in Myanmar amber
with surrounding material (including extended appendages) removed.
I=Basal cell; II=Suprabasal cell; III=Terminal cell; IV and V=Additional stalk cells
Bar=90 µm

Citation: Poinar Jr G (2016) A Mid-Cretaceous Ectoparasitic Fungus, Spheciophila adercia gen et sp. nov., Attached to a Wasp in Myanmar Amber.
Fungal Genom Biol 6: 145. doi:10.4172/2165-8056.1000145
Page 3 of 4
Volume 6 • Issue 2 • 1000145
Fungal Genom Biol
ISSN: 2165-8056 FGB, an open access journal
mm in length), the long multicellular stalk bearing numerous perithecia
and antheridia (Figure 3), the presence of a separate large tued branch
containing antheridial receptacle cells with developing endogenous
spermatia, and possessing ve stalk cells in a simple linear series
distinguishes the fossil from present day lineages of Laboulbeniales. Also,
the extended tued branch containing antheridial receptacle cells (Figure
4) is not found among the Laboulbeniales and while perithecia in the
Laboulbeniales are normally produced by cell II of the receptacle [6-13], in
Spheciophila adercia gen. et sp. nov., perithecia occur on the bent portion
of the extended stalk that arises from the top of stalk cell (Figure 3).
Holotype
Holotype female No. B-Hy-19 deposited in the Poinar amber
collection maintained at Oregon State University.
Etymology
e family and generic names are derived from the Greek
“sphecion”=small wasp and the Greek “philios”=loving. e specic
epithet is from the Greek “adercia”=unexpected.
Type locality
Myanmar (Burma), state of Kachin, Noije bum 2001 Summit Site
amber mine in the Hukawng Valley, SW of Maingkhwan (26º20´N,
96º36´E).
Type host
Wingless adult female ceraphronoid wasp (Hymenoptera:
Ceraphronoidea) [17] (Figure 1).
Discussion
Nourishment of Spheciophila adercia gen et sp. nov. was probably
obtained through the basal foot of the thallus that penetrated the cuticle
to reach the hemolymph. e thallus appears to be very well secured
and its prostrate position probably protected it from abrasion, although
the attened area on the terminal receptacle cell (Figure 3F) may be
where a secondary stalk was broken o. e recumbent orientation of
Spheciophila adercia gen et sp. nov. on its host is another character that
separates it from the Laboulbeniales, which are normally vertically or
sub-vertically positioned on their host [6,7].
Also separating it from the Laboulbeniales is the wasp host since
the only known hymenopteran hosts of Laboulbeniales are ants
(Hymenoptera: Formicidae) [7] and in general, Hymenoptera are very
infrequently parasitized by fungi [4,5]. It is obvious that Spheciophila
adercia gen et sp. nov. is a very unique fungus that may represent a stem
group of the Laboulbeniales since there are no other extant thallus-
bearing ectoparasitic fungi that develop on the integument of insects.
e wasp host, which was described as Aptenoperissus burmanicus, is
also quite bizarre and belongs to an extinct family in the superfamily
Ceraphronoidea [17].
Conclusion
In the past the Laboulbeniales was considered to be an enigmatic
lineage of insect symbionts and mycoparasites and the group was placed
in a number of dierent Orders and even Phyla [1]. In the scheme of
Hibbett et al. [18], the Laboulbeniales is placed in a separate Class
Laboulbeniomycetes, along with the Order Pyxidiophorales. However
Schoch et al. [19] later placed the Laboulbeniomycetes as a sister to
the Sordariomycetes and included the former with Sordariomyces
and Leotiomycetes in a clade (Sordariomyceta) comprising poricidal,
unitunicate taxa. It is not possible to determine whether Spheciophila
adercia gen. et sp. nov. belongs to one of the above orders, but chances
are good that it represents an early lineage of the Laboulbeniomycetes
since there are no other extant thallus-bearing ectoparasitic fungi that
develop on the integument of insects. Its discovery provides a rare
glimpse of an extinct lineage of ectoparasitic fungi attacking wasps
some 100 mya.
Acknowledgement
The author thanks the late Richard K. Benjamin (Rancho Santa Ana Botanic
Garden) and the late Isabelle I. Tavares (University of California, Berkeley)
for previous personal discussions on the morphology and systematics of the
Laboulbeniales. Thanks are also extended to Roberta Poinar and two anonymous
reviewers whose comments beneted the paper.
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Figure 4: Portion of the tufted branch of Spheciophila adercia gen. et sp.
nov. in Myanmar amber with maturing antheridial receptacle cells developing
endogenous spermatia.
Bar=23 µm. Insert shows detail of four maturing antheridial receptacle cells.
Bar=7 µm

Citation: Poinar Jr G (2016) A Mid-Cretaceous Ectoparasitic Fungus, Spheciophila adercia gen et sp. nov., Attached to a Wasp in Myanmar Amber.
Fungal Genom Biol 6: 145. doi:10.4172/2165-8056.1000145
Page 4 of 4
Volume 6 • Issue 2 • 1000145
Fungal Genom Biol
ISSN: 2165-8056 FGB, an open access journal
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Citation: Poinar Jr G (2016) A Mid-Cretaceous Ectoparasitic Fungus,
Spheciophila adercia gen et sp. nov., Attached to a Wasp in Myanmar Amber.
Fungal Genom Biol 6: 145. doi:10.4172/2165-8056.1000145
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